INVITED REVIEW

Current Trends in Extended Lymph Node

Dissection for Esophageal Carcinoma
Wen-Tao Fang, MD, Wen-Hu Chen, MD
Department of Thoracic Surgery
Shanghai Chest Hospital, Jiaotong University Medical School
Shanghai, China

ABSTRACT
Extended lymph node dissection helps increase the curativeness of resection, the
accuracy of surgical-pathological staging, and the prognosis of thoracic esophageal
carcinoma. However, it is also associated with significantly increased surgical
morbidity and has noticeable negative effects on the quality of life after surgery.
Current trends for selective lymph node dissection based on clinical evidence may be
helpful in reducing surgical risks while assuring the completeness of resection.

(Asian Cardiovasc Thorac Ann 2009;17:208–13)

KEYWORDS: Esophageal Neoplasms, Lymphatic Metastasis, Neck Dissection, Postoperative

Complications, Vocal Cord Paralysis

INTRODUCTION significantly. On the other hand, with metastatic nodes

Until now, radical resection has remained the most
effective means of cure for esophageal cancer. However,
the long-term outcome after routine esophagectomy
is far from satisfactory, with 5-year survival rates at
20%–30%.1–4 Lymph node status is one of the most
important prognostic factors for esophageal cancer.
Upon presentation with dysphagia, over 70% of patients
will already have lymph node metastasis.5 Of those who
survive surgery, 80% will eventually die from tumor
recurrence; at least 40% of these are due to recurrence in
lymph nodes.6 Therefore, esophageal carcinoma should
be considered at least as a local-regional disease, with all
the regional lymph nodes included, instead of a localized
lesion per se in the esophagus. Reducing local-regional
recurrence and thus improving the quality of life is as
important as gaining long-term survival.
MERITS OF EXTENDED LYMPH NODE
DISSECTION FOR ESOPHAGEAL CANCER
It has already been established that lymph nodes
metastasis from esophageal cancer may occur at an
early stage and skip to nodes far away from the primary
tumor.7–9 Theoretically, if all the involved regional
nodes could be completely removed along with the
tumor itself, the chance of cure would be increased, and
the risk of early local-regional recurrence reduced
left behind, not only might the disease be under-staged,
but the curativeness of surgery should also be ques-
tioned. Given that postoperative chemotherapy has
shown little survival benefit, and the lack of other
effective adjuvant therapies, it is not surprising to
observe a high recurrence rate in mediastinal or cervical
lymph nodes shortly after surgery.10,11 Such patients
often present with hoarseness or dyspnea caused by
depression of the recurrent laryngeal nerve or major
airway from enlarged lymph nodes. Apart from a dismal
survival, the quality of life in these patients is also
jeopardized.
While esophageal cancer is considered more or less a
systemic disease in Western nations, and treated mainly
with concurrent chemoradiotherapy, it is taken as a
local-regional disease in other parts of the world,
especially in Asian countries like Japan and China.
Based on this principle, clinical trials of systemic lymph
node dissection have been widely carried out since the
early 1980s. The extent of lymph node clearance was
first extended from the original mid and inferior
mediastinum to the superior mediastinum so as to
remove the lymph nodes along bilateral recurrent
laryngeal nerves. Then it was further extended into the
neck; lymph nodes along the cervical part of the

Fang Wen-Tao, MD Tel: +86 21 62821990 Fax: +86 21 68201190 Email: vwtfang@hotmail.com
Department of Thoracic Surgery, Shanghai Chest Hospital, 241 Huaihai Road West, Shanghai, 200030, China.
doi: 10.1177/0218492309103332
ß SAGE Publications 2009 Los Angeles, London, New Delhi and Singapore
ASIAN CARDIOVASCULAR & THORACIC ANNALS 208 2009, VOL. 17, NO. 2
Fang
recurrent nerves and those located lateral to the cervical
vessels were also dissected. Although the optimal extent
of lymph node clearance has always been under debate,
the superiority of extended lymphadenectomy has
rendered it a standard procedure in more than 70% of
institutions in Japan.7,12 It is also interesting to note that
quite a few leading institutions in Western nations have
also joined in the practice, with similar results to those
obtained in Japan, despite an increased incidence of
adenocarcinoma in their populations.13,14
The benefit of systemic lymph node dissection is based
mainly on 3 factors. Firstly, it provides more accurate
tumor staging. It was through systemic dissection that
lymph node metastasis was clinically proved to be a
common phenomenon in esophageal cancer. The
Japanese Association of Esophageal Oncology Group
carried out a nationwide survey on lymphadenectomy
among 96 institutions in 1991.7 The results showed that
the rate of lymph node metastasis was 58.7% after
2-field (thoraco-abdominal) dissection. It increased to
72.9% after adding cervical dissection, making the
procedure a 3-field (cervico-thoraco-abdominal) one.
It is noteworthy that apart from a 27.4% rate of cervical
metastasis, the rate of mediastinal metastasis was also
significantly increased from 40.8% after 2-field dissec-
tion to 55.8% after 3-field dissection, indicating more
thorough lymph node clearance in the superior medias-
tinum, especially the cervical-mediastinal junction.
At the same time, there was a significant upstaging of
the diseases after lymph node dissection was extended
further into the neck. The only prospective randomized
clinical trial comparing the results of 3-field and 2-field
dissections showed a 26% rate of cervical metastasis
from thoracic esophageal squamous cell carcinoma.12
It is worth mentioning that another clinical trial of
3-field dissection by Altorki and colleagues14 also
yielded a 70% regional lymph node metastasis rate
and a 35% cervical metastasis rate. In that trial,
however, the original lesions included both squamous
carcinoma and adenocarcinoma located in the distal
esophagus.
Secondly, the knowledge we now posses of the
characteristics of lymphatic metastasis from esophageal
cancer could not have been fully gained had it not been
for the practice of systemic dissection. The abundance of
lymphatics in the submucosal layer provides the
anatomical basis for lymph node metastasis from
esophageal cancer to occur at an early stage.15–17
According to the results of extended lymph node
dissection, regional node metastasis may reach
25%–30% when the tumor invades the submucosa, and
increases gradually with the depth of tumor invasion.7,8
The specific architecture of the lymphatics of the
submucosa also makes lymph flow more preferentially
2009, VOL. 17, NO. 2
Selective Lymphadenectomy
longitudinal rather than across the muscle layer of the
esophageal wall. Lymphs from above the carina mainly
go upward to the superior mediastinum and neck,
whereas lymphs below the carina go downward via the
mid and inferior mediastinum to the left gastric and
celiac nodes.17 Therefore, superior mediastinal nodes
are most commonly involved in upper esophageal
tumors, while mid-mediastinal nodes are most often
involved in middle esophageal tumors, and inferior and
abdominal nodes are most frequently involved in tumors
located in the lower third of the esophagus.9 Lymph
node stations most often involved in thoracic esophageal
carcinoma, such as the nodes along the cervical and
mediastinal part of the recurrent nerves, under the
carina, and at the peri-cardiac and left gastric artery,
may all be included as periesophageal nodes.
Thirdly, with more metastatic nodes removed at surgery,
the curativeness of resection has also been improved.
Although there have been few, if any, strictly designed
phase III trials comparing the long-term results of
lymph node dissection, the reported 5-year survival
rates after 3-field dissection have been without excep-
tion in the range of 40%–50%.7,8,13 On the contrary,
5-year survival rates after routine procedures such as
Ivor-Lewis or transhiatal esophagectomies seldom reach
over 30%.
The merit of removing all potentially involved lymph
nodes lies also in the fact that recurrence in local-
regional lymph nodes could be significantly reduced
after extended dissection. The quality of life for patients
is therefore improved dramatically. This has been
proved by studies of recurrence patterns after esopha-
gectomy (Table 1). A detailed review of the literature
revealed that although distant metastasis remained
unchanged, the rates of local-regional recurrence after
systemic nodal dissection, be it 2-field or 3-field, were
usually less than 20%, while it was in the range of 30%–
40% after routine esophagectomy.18–24 Kato and col-
leagues18 reported that similar rates of distant metastasis
occurred regardless of whether or not neck and superior
mediastinal nodes were removed (16% and 17%).
However, with 3-field dissection, local recurrence was
reduced to 17% in contrast to routine esophagectomy
which was as high as 38%. It was noteworthy that
relapse in mediastinal nodes was reduced from 23% to
11%, and in cervical nodes from 12% to 2%. The
autopsy study by Katayama and colleagues25 also
revealed that local recurrence was significantly lower
after subtotal esophagectomy with lymph node dissec-
tion (19.4%) than a partial esophagectomy per se
(66.7%). The benefit of reducing local recurrence is
also possibly in the management of adenocarcinoma of
the esophagus. Hagen and colleagues21 found that
among 10 local-regional relapses in 100 esophageal
209 ASIAN CARDIOVASCULAR & THORACIC ANNALS
Selective Lymphadenectomy Fang

adenocarcinomas after systemic dissection, only 1
occurred within the region of dissection, and the other
9 beyond it. Clark and colleagues23 reported that for 15
regional nodal relapses in 38 adenocarcinomas located
in the distant esophagus and gastric cardia, 60% were
beyond the region of dissection, indicating that exten-
sion of nodal dissection might have decreased local
recurrence after surgery.
DISADVANTAGES OF 3-FIELD DISSECTION
Although there is now less doubt about the benefits of
extended lymph node dissection, the optimal extent of
dissection has always been controversial.12,25,26 As with
similar procedures in the management of other malig-
nancies, systemic dissection is a double-bladed sward.
The greater the extent of dissection, the better the
prognosis and local control might be; but the higher
would be the surgical risks. If the mortality rates have
been repeatedly reported to be similar, it is mainly
because almost all of these reports were based on
historical controls.7,12,25 In fact, complications directly
related to surgical maneuvers, such as recurrent nerve
palsy and anastomotic leakage, are far more common
after 3-field dissection than after 2-field dissection
(Table 2). In a parallel study comparing the results
from 2 referral centers in Japan and China in the same
time period, the overall morbidity rate was 64% after
3-field dissection, significantly higher than the 41.7%
after 2-field dissection.27
Recurrent laryngeal nerve palsy is the most often
mentioned complication directly related to cervical
and superior mediastinal dissection. In the above-
mentioned national survey by the Japanese Association
of Esophageal Oncology Group, the only significantly
increased postoperative complication after 3-field dis-
section was recurrent nerve paralysis.7 In one of the few
controlled studies comparing different extents of nodal
dissection, an astounding 53% rate of tracheotomy after
3-field dissection was documented. In a prospective
trial, Fang and colleagues28 also found a significantly
higher rate of recurrent nerve palsy in the 3-field group
(22.9%) than in the 2-field group (9.6%). Furthermore,
they noticed that it was significantly related to anasto-
motic leakage (53.8% vs. 13.5%), another major
problem in most reports concerning 3-field dissection.
The reason for this relationship was attributed to the
increased but ineffective cough in patients having
recurrent nerve injury during dissection. This may
cause incessant compression on the stomach located in
the anterior mediastinum and hence increased tension on
the cervical anastomosis.29 They also found increased
(although not significantly) pulmonary and cardiac
complications after 3-field dissection compared to
2-field dissection. Besides, recurrent nerve palsy
would have a significant impact on quality of life in
the long run, in terms of speech, swallowing, and
respiratory functions.30 All these have become major
obstacles to an even wider application of extended nodal
dissection.

Table 1. Recurrence patterns after esophagectomy with or without lymph node dissection

Lymph Node Recurrence

No. of Extent of Overall Distant Local
Author Cases Dissection Recurrence Metastasis Recurrence Neck Chest Abdomen
18
Kato 160 3-field 36.8% 49% 18%
Nakagawa19 171 3-field 43.3% 16.9% 20.3%
Dresner20 212 2-field 42% 18% 23% 2% 3% 3%
Hagen21 100 2-field 31% 10%
Hulscher22 137 Transhiatal 52.6% 29.2% 37.3% 8%
Clark23 38 Sampling 53% 40% 7.9% 21% 24%
Katayama24 43 Dissection 62.8% 39.5% 19.4% 11.6% 37.2% 16.3%
(autopsy) Sampling 66.7%

Table 2. Surgical morbidity in 2-field and 3-field lymph node dissection

Isono7 Fang27 Kato12

Variable (Questionnaire Survey) (Comparative Study) (Controlled Study)
Extent of dissection 3-field 2-field 3-field 2-field 3-field 2-field
No. of cases 1,791 2,799 50 48 77 73
Overall morbidity 53.9% 56.0% 64.0% 41.7% 62.3% 75.3%
Recurrent nerve palsy 20.3% 14.0% 10.0% 14.0% 14.3% 20.5%
Anastomotic leakage 36.0% 22.9% 33.8% 23.3%

ASIAN CARDIOVASCULAR & THORACIC ANNALS 210 2009, VOL. 17, NO. 2
Fang
CURRENT TREND TOWARD SELECTIVE
APPROACHES IN LYMPH NODE DISSECTION
Esophageal squamous cell carcinoma bears a significant
similarity to breast cancer in that the prognosis is largely
depended on the regional lymph node status. For a long
time, nodal status of breast cancer was determined by
axillary lymph node dissection, which was also asso-
ciated with significant morbidity. Therefore, a reason-
able selection of dissection extent so as to diminish the
surgical risks while still assuring the completeness of
resection is the key to the problem. As with the situation
in the management of breast cancer in recent years, there
is also a trend toward limited lymph node dissection in
the surgical treatment of esophageal cancer.
In a well-presented review of the merits and demerits of
lymph node dissection, Law and Wong26 proposed that
2-field dissection might be enough. There were 2
reasons supporting this hypothesis. First, patients with
cervical metastasis had such a poor prognosis that this
subgroup might not benefit from the additional dissec-
tion. However, this has been repeatedly disproved.
Occult cervical metastasis carries a different prognosis
from palpable neck lymphadenopathy. Tachimori and
colleagues31 reported that after 3-field dissection, the 3-
year survival of patients with occult cervical lympha-
denopathy reached 43.8%, and it was significantly better
than the survival rate in patients with palpable cervical
nodes. Fang and colleagues28 also reported that 2-year
survival of patients with impalpable cervical metastasis
could reach 50%, comparable to that in patients with
local nodal disease only. The second reason for
confining the extent of dissection to the thoracoabdom-
inal region is that most cervical metastases are along the
recurrent nerve chain and might be dissected through the
chest. Technically, lymph nodes along the right recur-
rent nerve can be easily removed from the thoracic
cavity. However, lymph nodes at the left cervical-
thoracic junction are far more difficult to access during
the chest maneuver. Unfortunately, the metastasis rate
on both sides are almost similar for thoracic esophageal
lesions.8,9
Therefore, 3-field dissection should not be abandoned,
but it should be carried out reasonably so as to tailor
the procedure to patients individually. The underlying
philosophy is to minimize the surgical risks while still
retaining the merits of lymph node dissection. Attempts
have already been made in several ways to pursue
selective approaches in 3-field lymphadenectomy.28,32–34
Firstly, most studies on lymph node metastasis in
esophageal cancer revealed that the extent of lymphatic
involvement is related to the depth of tumor invasion.
Early superficial cancers confined to the mucosa seldom
metastasis to cervical nodes, and thus could be exempted
from cervical dissection. However, this would apply
2009, VOL. 17, NO. 2
Selective Lymphadenectomy
only to a very small proportion of surgical candidates,
as most patients presenting with symptoms would
already be in a locally advanced stage. Even tumors
invading only the submucosal layer would have a
cervical metastasis rate of over 15%.32 Secondly,
according to the current edition of the International
Union Against Cancer classification for esophageal
cancer, cervical lymphadenopathy is defined as M1a
for tumors located at the upper thoracic esophagus, and
as M1b for those located at the middle and lower
esophagus, indicating a possibly different prognostic
significance. So far there is no evidence that cervical
dissection would be beneficial to upper esophageal
tumors only. On the contrary, metastasis to the neck
lymph nodes is equally common in tumors located at the
upper and middle esophagus.33 As mentioned above,
even for adenocarcinomas at the lower third of the
esophagus, metastasis could reach 30%.14 Thirdly, as
with the recent trends in breast cancer surgery, a
‘‘sentinel lymph node’’ is another appealing proposal.34
However, esophageal cancer contrasts anatomically
with breast cancer in the means of lymphatic drainage.
Until now, it has been impossible to identify a sentinel
nodal station for cervical metastasis. Besides, it is
technically unfeasible to add a second-stage cervical
dissection if the anastomosis was located high in the
neck during the first-stage operation, instead of an
intrathoracic anastomosis as proposed by Noguchi and
colleagues.34
In addition, selective lymph node dissection based on
preoperative ultrasonography seems to be a more
rational proposal. It has already been used in the surgical
management of other malignancies such as melanoma,
breast cancer, and head and neck cancers.35–37 Fang and
colleagues28 proposed selective neck dissection based
on cervical ultrasonography because the sensitivity and
accuracy of ultrasonography for impalpable cervical
lymphadenopathy could be as high as 80%–90%.31,38,39
Nearly 60% of their patients with negative ultrasono-
graphy were spared the more invasive neck dissection
and thus the potential morbidities including recurrent
laryngeal nerve palsy. The yield of metastatic cervical
nodes (19.5%) was in the same range as in the series of
Tachimori and colleagues31 (22.9%) where all patients
received neck dissection irrespective of the result of
ultrasonography.
For ethical reasons, it is impossible to carry out
prospectively randomized studies comparing the results
of selective 3-field dissection with routine 3-field
dissection. However, in recent years there has been
accumulating evidence suggesting a trend toward a
reasonable selection of dissection. Contemplation of a
surgical indication should always take into consideration
both the progressiveness of the tumor and the patients’
211 ASIAN CARDIOVASCULAR & THORACIC ANNALS
Selective Lymphadenectomy
tolerance of the procedure. The solution to these
problems lies in how to select appropriate candidates
for 3-field dissection so as to maximize the benefits
and minimize the risks, rather than to linger on the
so-called optimal extent of dissection. Future studies are
expected to add more evidence and help elucidate the
problem.
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